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Marine Biology

, Volume 153, Issue 4, pp 579–588 | Cite as

Evidence of abalone (Haliotis rubra) diet from combined fatty acid and stable isotope analyses

  • M. A. Guest
  • P. D. Nichols
  • S. D. Frusher
  • A. J. Hirst
Research Article

Abstract

Abalone are common herbivores throughout temperate and tropical waters, and yet the contribution of red and brown macroalgae to the diet of wild abalone remains unclear. In the northern hemisphere, adult abalone are considered to consume predominantly brown algae, but in the southern hemisphere abalone are thought to prefer red algae. Conventional methods such as gut content analysis and feeding trials provide some insight into diet choice, but the associated biases of these techniques create uncertainty surrounding the aforementioned variability in abalone diet. We use combined stable isotope and fatty acid analysis to determine the relative contribution of red algae, brown algae and detritus/microalgae to the diet of wild abalone in Tasmanian waters. Stable isotopes of carbon suggest that brown algae and/detritus are a more important source of carbon than red algae. Fatty acid analysis confirmed the larger contribution of brown algae to the diet of abalone, and also identified the bacterial and diatom component of detritus to be an important contributor to abalone diet. These results show combined use of chemical tracers to be a promising technique for resolving abalone diet, and challenge current perceptions regarding spatial variability in abalone diet choice.

Keywords

Detritus Carbon Isotope Macroalgae Fatty Acid Profile Brown Alga 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank B. Connell, S. Fava, S. Ibbott, and R. Kilpatrick for assistance in the field. Thanks to G. Edgar and J. Valentine who helped with identification of red algae species. The assistance of B. Mooney, M. Miller, K. Wheatley with laboratory processing and interpretation of fatty acid profiles were especially helpful. Thanks to J. Oakes for advice with analysis of detrital samples. D. Holdsworth managed the CSIRO GC-MS facility. Advice from A Revill was useful in modelling and interpretation of stable isotope values. Comments on the manuscript by C. Mundy, S. Shepherd and two anonymous reviewers are appreciated and helped to improve the manuscript. Thanks to M. Morffew for creating the map.

References

  1. Ackman RG, Hooper SN (1973) Non-methylene-interrupted fatty acids in lipids of shallow-water marine invertebrates: a comparison of two molluscs (Littorina littorea and Lunatia triseriata) with the sand shrimp (Crangon septemspinosus). Comp Biochem Physiol 46B:153–165Google Scholar
  2. Barkai R, Griffiths CL (1986) Diet of South African abalone Haliotis midae. S Afr J Mar Sci 4:37–44CrossRefGoogle Scholar
  3. Best NJ, Bradshaw CJA, Hindell MA, Nichols PD (2003) Vertical stratification of fatty acids in the blubber of southern elephant seals (Mirounga leonine): implications for diet analysis. Comp Biochem Physiol 134B:253–263CrossRefGoogle Scholar
  4. Christie WW (1982) Lipid analysis. Pergamon Press, OxfordGoogle Scholar
  5. Connolly RM, Hindell JS, Gorman D (2005) Seagrass and epiphytic algae support nutrition of a fisheries species Sillago schomburgkii in adjacent intertidal habitats. Mar Ecol Prog Ser 286:69–79CrossRefGoogle Scholar
  6. Dalsgaard J, St John M, Kattner G, Muller-Navarra K, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefGoogle Scholar
  7. Dalsgaard J, St John M (2004) Fatty acid biomarkers: validation of food web and trophic markers using 13C-labelled fatty acids in juvenile sandeel (Ammodytes tobianus). Can J Fish Aquat Sci 61:1671–1680CrossRefGoogle Scholar
  8. Day RW, Cook P (1995) Bias towards brown algae in determining diet and food preferences: the South African abalone Haliotis midae. Mar Freshwat Res 46:623–627CrossRefGoogle Scholar
  9. Deagle BE, Jarman SN, Pemberton D, Gales NJ (2005) Genetic Screening for Prey in the Gut Contents from a Giant Squid (Architeuthis sp.). J Hered 96:417–423CrossRefGoogle Scholar
  10. Deagle B, Tollit D (2006) Quantitative analysis of prey DNA in pinniped faeces: potential to estimate diet composition? Conserv Genet 8:743–747CrossRefGoogle Scholar
  11. Dunstan GA, Volkman JK, Barrett SM, LeRoi JM, Jeffrey SW (1994) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155–161CrossRefGoogle Scholar
  12. Dunstan GA, Baillie HJ, Barrett SM, Volkman JK (1996) Effect of diet on the lipid composition of wild and cultured abalone. Aquaculture 140:115–127CrossRefGoogle Scholar
  13. Edgar GJ, Barrett NS (1997) Short term monitoring of biotic change in Tasmanian Marine Reserves. J Exp Mar Biol Ecol 213:261–279CrossRefGoogle Scholar
  14. Edgar GJ, Barrett NS (1999) Effect of the declaration of marine reserves on Tasmanian reef fishes, invertebrates and plants. J Exp Mar Biol Ecol 242:107–144CrossRefGoogle Scholar
  15. Erasmus JH, Cook PA, Coyne VE (1997) The role of bacteria in the digestion of seaweed by the abalone Haliotis midae. Aquaculture 55:377–386CrossRefGoogle Scholar
  16. Farquhar GD, Ehlerlinger JR, Hubrick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  17. Fenton GE, Ritz DA (1988) Changes in carbon and hydrogen stable isotope ratios of macroalgae and seagrass during decomposition. Estuar Coast Shelf Sci 26:429–436CrossRefGoogle Scholar
  18. Fenton GE, Ritz DA (1989) Spatial variability of 13C:12C and D:H in Ecklonia radiata (C.Ag.) J. Agardh (Laminariales). Estuar Coast Shelf Sci 28:95–102CrossRefGoogle Scholar
  19. Fleming AE (1995) Digestive efficiency of the Australian abalone Haliotis rubra in relation to growth and feed preference. Aquaculture 134:279–293CrossRefGoogle Scholar
  20. Foale S, Day R (1992) Recognisability of algae ingested by abalone. Aust J Mar Freshw Res 43:1331–1338CrossRefGoogle Scholar
  21. Gee JM (1989) An ecological and economic review of meiofauna as food for fish. Zool J Linn Soc 96:243–261CrossRefGoogle Scholar
  22. Grubert MA, Dunstan GA, Ritar AJ (2004) Lipid and fatty acid composition of pre- and post-spawning blacklip (Haliotis rubra) and greenlip (Haliotis laevigata) abalone conditioned at two temperatures on a formulated feed. Aquaculture 242:297–311 CrossRefGoogle Scholar
  23. Guest MA, Connolly RM, Loneragan NR (2004) Within and among-site variability in delta C-13 and delta N-15 for three estuarine producers, Sporobolus virginicus, Zostera capricorni, and epiphytes of Z-capricorni. Aquat Bot 79:87–94CrossRefGoogle Scholar
  24. Johns RB, Nichols PD, Perry GJ (1979) Fatty acid composition of ten marine algae from Australian waters. Phytochemistry 18:799–802CrossRefGoogle Scholar
  25. Leighton D, Boolootian RA (1963) Diet and growth in the Black Abalone Haliotis cracerodii. Ecology 44:227–238CrossRefGoogle Scholar
  26. Lewis T, Nichols PD, McMeekin TA (2000) Evaluation of extraction methods for recovery of fatty acids from lipid-producing microheterotrophs. J Microbiol Methods 43:107–116CrossRefGoogle Scholar
  27. Lindberg DR (1992) Evolution, distribution and systematics of Haliotidae. In: Shepherd SK, Tegner MJ, Guzman Del Proo SA (eds) Abalone of the world. Fishing News Books, Carlton, pp 169–181Google Scholar
  28. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390CrossRefGoogle Scholar
  29. McShane PE, Gorfine HK, Knuckey IA (1994) Factors influencing food selection in the abalone Haliotis rubra (Mollusca: Gastropoda). J Exp Mar Biol Ecol 176:27–37CrossRefGoogle Scholar
  30. Melville AJ, Connolly RM (2003) Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136:499–507CrossRefGoogle Scholar
  31. Miller LP, Gaylord B (2007) Barriers to flow: the effects of experimental cage structures on water velocities in high-energy subtidal and intertidal environments. J Exp Mar Biol Ecol 344:215–228CrossRefGoogle Scholar
  32. Nelson MM, Leighton DL, Phleger CF, Nichols PD (2002) Comparison of growth and lipid composition in the green abalone, Haliotis fulgens, provided specific macroalgal diets. Comp Biochem Physiol 131B:695–712CrossRefGoogle Scholar
  33. Peterson BJ (1999) Stable isotopes as tracers of organic matter input and transfer in benthic food webs: a review. Acta Oecologica 20:479–487CrossRefGoogle Scholar
  34. Peterson BJ Fry B (1987) Stable isotopes in ecosystem studies. Ann Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  35. Peterson CH, Black R (1994) An experimentalist’s challenge: when artefacts of intervention interact with treatments. Mar Ecol Prog Ser 111:289–297CrossRefGoogle Scholar
  36. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179 (see also erratum Oecologia 128:204)CrossRefGoogle Scholar
  37. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269CrossRefGoogle Scholar
  38. Phillips KL, Nichols PD, Jackson GD (2003a) Temporal variations in the diet of the squid Moroteuthis ingens at Macquarie Island: stomach contents and fatty acid analyses. Mar Ecol Prog Ser 256:135–149CrossRefGoogle Scholar
  39. Phillips KL, Nichols PD, Jackson GD (2003b) Size-related dietary changes observed in the squid Moroteuthis ingens at Falkland Islands: stomach contents and fatty acid analyses. Polar Biol 26:474–485Google Scholar
  40. Phleger CF, Nelson MN, Groce AI, Cary SC, Coyne KJ, Nichols PD (2005a) Lipid composition of deep sea hydrothermal vent tubeworms Riftia pachyptila, crabs Munidopsis subsquamosa and Bythograea thermydron, mussels Bathymodiolus sp. and limpets Lepetodrilus spp. Comp Biochem Physiol 141B:196–210CrossRefGoogle Scholar
  41. Phleger CF, Nelson MN, Groce AI, Cary SC, Coyne KJ, Gibson JAE, Nichols PD (2005b) Lipid composition of deep sea hydrothermal vent polychaetes Alvenella pompejana, A. caudate, Paralvinella grasslei and Hesiolyra bergii. Deep Sea Res I 52:2333–2352CrossRefGoogle Scholar
  42. Prince J (1989) The fisheries biology of the Tasmanian stocks of Haliotis rubra. PhD Thesis, University of Tasmania, pp 60–70Google Scholar
  43. Raven JA, Johnston AM, Kubler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378CrossRefGoogle Scholar
  44. Shepherd SA (1973) Studies on southern Australian abalone (genus Haliotis). 1. Ecology of five sympatric species. Aust J Mar Freshw Res 24:217–257CrossRefGoogle Scholar
  45. Shepherd SA (1975) Distribution, habitat and feeding habits of abalone. Aust Fish 34:12–15Google Scholar
  46. Shepherd SK, Steinberg PD (1992) Food preferences of three Australian abalone species with a review of the algal food of abalone. In: Shepherd SK, Tegner MJ, Guzman Del Proo SA (eds) Abalone of the world. Fishing News Books, Carlton, pp 169–181Google Scholar
  47. Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Funct Ecol 19:751–762CrossRefGoogle Scholar
  48. Steinberg PD (1989) Biogeographical variation in brown algal polyphenolics and other secondary metabolites: comparison between temperate Australasia and North America. Oecologia 78:373–378CrossRefGoogle Scholar
  49. Stephenson RL, Tan FC, Mann KH (1984) Stable carbon isotope variability in marine macrophytes and its implications for food web studies. Mar Biol 81:223–230CrossRefGoogle Scholar
  50. Stephenson RL, Tan FC, Mann KH (1986) Use of stable carbon isotope ratios to compare plant material and potential consumers in a seagrass bed and a kelp bed in Nova Scotia, Canada. Mar Biol 30:1–7Google Scholar
  51. Su XQ, Antonas KN, Li D (2006) Comparison of n-3 polyunsaturated fatty acid contents of wild and cultured Australian abalone. Int J Food Sci Nutr 55:149–154CrossRefGoogle Scholar
  52. Vanderklift MA (2002) Interactions between sea urchins and macroalgae in south-western Australia: testing general predictions in a local context. PhD Thesis, University of Western Australia, PerthGoogle Scholar
  53. Virtue P, Nichols PD, Nichol S, McMinn A, Sikes EL (1993) The lipid composition of Euphausia superba Dana in relation to the nutritional value of Phaeocystis pouchetii (Hariot) Lagerheim. Antarct Sci 5:169–177CrossRefGoogle Scholar
  54. Volkman JK, Johns RB, Gillan FT, Perry GJ, Bavor HJ Jr (1980) Microbial lipids of an intertidal sediment. I. Fatty acids and hydrocarbons. Geochem Cosmochim Acta 44:113–1143CrossRefGoogle Scholar
  55. Volkman JK (1986) A review of sterol markers for marine and terrigenous organic matter. Org Geochem 9:83–99CrossRefGoogle Scholar
  56. Wells FE, Keesing JK (1989) Reproduction and feeding in the abalone Haliotis roei Gray. Aust J Mar Freshw Res 40:187–197CrossRefGoogle Scholar
  57. Winter FC, Estes JA (1992) Experimental evidence for the effects of polyphenolic compounds from Dictyoneurum californicum Ruprecht (Phaeophyta: Laminariales) on the feeding rate and growth in the red abalone Haliotis rufescens Swainson. J Exp Mar Biol Ecol 155:263–277CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • M. A. Guest
    • 1
  • P. D. Nichols
    • 2
    • 3
  • S. D. Frusher
    • 1
  • A. J. Hirst
    • 1
  1. 1.Tasmanian Aquaculture and Fisheries InstituteTaroonaAustralia
  2. 2.CSIRO Marine and Atmospheric ResearchHobartAustralia
  3. 3.Antarctic and Climate EcosystemsUniversity of TasmaniaHobartAustralia

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